Analysis of multiparasitism by Eupelmus vuilleti (Craw) (Eupelmidae) and Dinarmus basalis (Rond) (Pteromalidae) in the presence of one of their common hosts,Bruchidius atrolineatus (Pic) (Coleoptera Bruchidae)

Bruchidius atrolineatus (Pic) is a tropical beetle (Coleoptera Bruchidae) that develops during the larval and pupal stages in the seeds of a legume Vigna unguiculata (Walp). Two species of Hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Craw), solitary ectoparasitoids of the larvae and pupae of B. atrolineatus, were introduced successively in the presence of their hosts, varying the interval between the two introductions. When D. basalis females were introduced 24 h, 3 days or 7 days after E. vuilleti, multiparasitism was low. The females had low fecundity, and their eggs were not distributed randomly over the different available hosts. When E. vuilleti females were introduced second, they oviposited on the different hosts availabe and did not avoid multiparasitism. The presence of hosts already parasitised by D. basalis increased the reproduction of E. vuilleti, and the fecundity of the females was higher than in control batches with E. vuilleti alone. E. vuilleti seems capable of detecting the ovipositor shafts drilled by the D. basalis females, and by introducing its own ovipositors killing the D. basalis eggs or larvae. When interspecific competition was occurring the number of E. vuilleti adults emerging from the seeds was no different from that observed in control batches with E. vuilleti alone, and there were always fewer D. basalis adults than in control batches (D. basalis alone). This interspecific competition reduces the influence of the two parasitoids in the biological control of bruchid populations.     

Sex ratio regulation in the waspEupelmus vuilleti (crwf.), an ectoparasitoid on bean weevil larvae (Hymenoptera: Pteromalidae)

In Africa, the seeds and/or pods ofVigna unguiculata andVigna radiata (Papilionacea) are attacked in fields and storage structures by bruchid beetlesCallosobruchus maculatus andBruchidius atrolineatus, on which parasitoid communities can develop. One of these parasitoids is the solitary ectoparasitoidEupelmus vuilleti (Eupelmidae). The storage conditions ofV. unguiculata andV. radiata favor the overlapping of all host stages during several months. These conditions suggest that female parasitoids would vary the sex ratio of their offspring according to the different sizes or developmental stages of hosts. The sex ratio ofE. vuilleti was strongly related to the developmental stage of the hostC. maculatus. Under our experimental conditions, where superparasitism is rare, the proportion of daughters varied between 5 and 25% on the third larval stage but reached 70 to 90% on the pupae. The increase in the proportion of daughters was also observed in the absence of superparasitism. In this case, there was an absolute coincidence between the sex ratio of eggs laid and that of emerged adults. Manipulation of the sex of the egg by the females seems to take place at the time of the egg's fertilization. The relation between host weight and egg sex showed that the male eggs are preferentially laid on lighter host larvae and the female eggs on heavier ones.     

Interspecific competition betweenEupelmus vuilleti andDinarmus basalis, two solitary ectoparasitoids ofBruchidae larvae and pupae

Coexistence of two solitary ectoparasitoids of bruchids may be the result of counter-balanced competition. Some strategies in interspecific competition at the extrinsic level of female behaviour are identified.Dinarmus basalis (Rondani) (Hymenoptera; Pteromalidae) has adapted an evasion strategy to avoid competition. Females ofD. basalis show interspecific discrimination against hosts parasitized byEupelmus vuilleti Crawford (Hymenoptera; Eupelmidae) and lay fewer eggs in the presence of females or hosts parasitized by the latter.Eupelmus vuilleti has adapted an aggressive strategy. In contrast toD. basalis, E. vuilleti concentrates her ovipositions on hosts already parasitized byD. basalis. Females ofE. vuilleti preferably use oviposition holes made by other parasitoids, and are able to kill eggs and larvae ofD. basalis selectively by thrusts of their ovipositor (ovicide and larvicide). Furthermore,E. vuilleti can act as a facultative hyperparasitoid on older larvae ofD. basalis. The number ofE. vuilleti offspring is not affected by the presence ofD. basalis on a host. Our study does not provide insight in the process of larval competition.

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Résumé La coexistence de deux ectoparasito?des solitaires de Bruchidés peut resulter de compétition contrebalancée (Zw?lfer, 1971). Quelques stratégies en situation de compétition interspécifique ont été indentifiées au niveau (extrinsèque) du comportement de femelles.Dinarmus basalis (Rondani) (Hymenoptera; Pteromalidae) a développé une stratégie d'évitement de la compétition. Les femelles deD. basalis montrent une capacité à reconna?tre les h?tes parasités parEupelmus vuilleti Crawford (Hymenoptera; Eupelmidae), et pondent moins d'œufs en présence des femelles d'E. vuilleti ou des h?tes parsités par cette espèce.Eupelmus vuilleti a adapté une stratégie aggressive. Au contraire deD. basalis, E. vuilleti concentre sa ponte sur les h?tes déjà parasités parD. basalis. Les femelles d'E. vuilleti utilisent préférentiellement les orifices de ponte pratiqués par les autres parasito?des. Elles sont alors capables de tuer grace à l'ovipositeur les œufs et les larves deD. basalis (ovicide et larvicide). De plus,E. vuilleti est capable d'hyperparasiter les larves de dernier stade deD. basalis. Le nombre de descendants d'E. vuilleti n'est pas affecté par la présence deD. basalis sur un h?te. Notre étude expérimentale n'a pas permis l'étude du mécanisme de la compétition larvaire.

     

Hyperparasitisme facultatif de parasitoïdes en cours de développement par les femelles des ectoparasitoïdes Eupelmus vuilleti et Eupelmus orientalis Craw

In a community of three ectoparasitoids, Dinarmus basalis, Eupelmus vuilleti and E. orientalis, the host Callosobruchus maculatus parasitised 48 h before by D. basalis, is accepted by E. vuilleti females after they have eliminated the eggs and neonatal larvae of D. basalis. This ovicidal and larvicidal behaviour enables E. vuilleti to develop on C. maculatus instead of D. basalis. E. vuilleti females are able to parasitise the L5 larval stage and the pupa of D. basalis: their larvae therefore feed at the expense of the developing parasitoid. This trophic level is that of hyperparasitism. However, E. vuilleti females rarely practise hyperparasitism on their own L5 larvae and on those of E. orientalis. This behaviour reveals a high behavioural plasticity enabled by intra- and interspecific recognition of parasitoids used as hosts. Hyperparasitism activity in E. orientalis females is higher than that in E. vuilleti females since they hyperparasitise host parasitoids more frequently without preferential species choice. However, E. vuilleti seems to be free from competitive pressure with E. orientalis, as the former penetrates deeply into a grain store contaminated with C. maculatus in contrast to E. orientalis females, which remain on the surface from where they escaped.     

Oviposition strategy of the parasitic waspDinarmus basalis (Hymenoptera,Pteromalidae)

Summary Host type choice and sex allocation were examined using the solitary parasitic waspDinarmus basalis (Pteromalidae, Hymenoptera) parasitizing larvae or pupae of the bean weevilCallosobruchus chinensis (Bruchidae, Coleoptera) within azuki beans (Vigna angularis). The wasps were offered two types of host; one was hard for the mother to lay eggs in, but was more beneficial for the offspring; the other was easy for the mother to lay eggs in, but was less beneficial for the offspring. The two types of host were one large host (17-day old host) in one bean and 6 small hosts (12-, or 13-day old hosts) in one bean. The same number of each host was presented at the same time to female wasps. The wasps accepted more 17-day old hosts than 12-day old hosts, and more 13-day old hosts than 17-day old hosts in each pair-wise choice experiment. The proportions of accepted host types were different from the proportions predicted by optimization models of random prey encounter with known or unknown prey densities. The wasps showed partial preference of host types. Incomplete information about prey densities, and about the costs and benefits of the two types of host may have generated the partial preference. Two predictions of host sizemodels, that (1) there should be a negative relationship between host size and offspring sex ratio (proportion of male offsprings), and (2) the sex ratio in each size host changes with the relative frequency of each size host utilized, were qualitatively supported.     

Sperm Storage and Use After Multiple Mating in Dinarmus basalis (Hymenoptera: Pteromalidae)

Multiple mating and its effects on the sex ratio in Dinarmus basalis (Hymenoptera: Chalcidoidea, Pteromalidae), an ectoparasitoid of Callosobruchus maculatus (Coleoptera: Bruchidae), were investigated under controlled conditions. Once-mated females suffer a sperm depletion about 21 days after mating and thereafter are constrained to produce only haploid males. On the other hand, three-times-mated females store more sperm in their spermathecae (335 vs 147) and produce daughters during the major part of their reproductive life. Consequently, once-mated females showed a male-biased life time sex ratio (mean = 0.31) as opposed to three-times-mated females (mean = 0.63). Females can copulate only at the beginning of their reproductive life, and multiple mating must occur before egg-laying activity. This behavioral strategy could be an avoidance of consanguinity in a promiscuous environment. This ectoparasitoid species reveals a reproductive strategy which promotes polyandry and a very high sperm efficiency.     

Sex Allocation Decision Under Superparasitism by the Parasitoid Wasp Eupelmus vuilleti

Superparasitism is a widespread phenomenon in parasitoids and may be advantageous in some circumstances. In this study, offspring sex ratio was analysed in three superparasitism situations: when the second egg was laid by a random Eupelmus vuilleti (Hymenoptera: Eupelmidae) female from a group, when an isolated female was allowed to lay two eggs on the same host (self-superparasitism) or laid one egg on a host already parasitized by a conspecific (conspecific superparasitism). Females produced a different offspring sex ratio according to the different superparasitism situations tested. These sex ratios are in line with the local mate competition theory. The results further suggest that females can discriminate between hosts parasitized by a conspecific or by themselves and adapt the sex of the eggs they lay accordingly.     

Egg Deposition Behavior in the Haplodiploid Sawfly Athalia rosae ruficornis Jakovlev (Hymenoptera: Symphyta: Tenthredinidae)

The egg deposition behavior of the turnip sawfly, Athalia rosae (Hymenoptera: Symphyta), is described. Both unmated and mated females lay eggs individually inside of fresh young leaves of cruciferous plants. During an oviposition event, females exhibit a distinct pause in abdominal contractions just before the actual egg deposition act. Unmated females show a longer pause (11.31 s on average) than mated females (4.38 s on overall average). By employing an eye color mutation, the sex of the eggs laid by females was ascertained. Females mated once lay mostly fertilized (diploid female) eggs initially but begin to lay a considerable number of unfertilized (haploid male) eggs later in life. The laying of an unfertilized egg is associated with a longer pause (6.98 s on average) than the laying of a fertilized egg (3.76 s on average). These results are in contrast to previous reports on apocritan Hymenoptera, where the presence of a pause or a longer pause during oviposition was associated with the deposition of fertilized eggs rather than unfertilized eggs. The possibility that mated Athalia rosae females control fertilization and its implications for sex allocation strategies are discussed.     

‘Males second’ strategy in the allocation of sexes by the parasitic wasp,Gryon japonicum

Summary Patterns of the sex ratio allocation of Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae), a solitary egg parasitoid of Riptortus clavatus (Thunberg) (Heteroptera: Alydidae), were investigated in the laboratory, and the result was checked against the field data on the sex composition of the parasitoid. When five host eggs were presented simultaneously to each of the females of G. japonicum in a laboratory experiment, they had a strong tendency to lay a male egg in second host egg and female eggs in the others. However, when four host eggs were presented to each female more than 3 h after the completion of oviposition on a host egg, most of the females laid male eggs in the third oviposition, i.e. the second host eggs after the experimental interruption of oviposition. These results indicated that there was a mechanism for G. japonicum to produce a male egg in the second host egg in consecutive ovipositions, and that the mechanism was reset by more than 3 h intervals of oviposition. By this mechanism, G. japonicum is thought to produce the precise sex ratio in response to the size of a host egg batch. Field data on the size of a host egg batch and the sex composition of the parasitoid in a host egg batch supported this view.     

The life history continuum hypothesis links traits of male ants with life outside the nest

Biological control of bruchid beetles, Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae), infesting cowpea seeds, Vigna unguiculata (L.) Walpers (Fabaceae), can be performed via augmentative releases of Dinarmus basalis Rondani (Hymenoptera: Pteromalidae) parasitoid wasps. Females of the latter species are therefore likely to experience intense intraspecific competition: they should encounter numerous previously parasitized hosts but also conspecific competitors, with which they may fight to secure hosts on which to lay their eggs. Such contests might therefore disrupt biological control programs. Here, we studied aggressive behavior that D. basalis females show toward conspecific competitors and subsequent host exploitation strategies. We further investigated factors that classically affect contest intensity and outcomes in animals, such as the effect of ownership status, by manipulating the residency period before the intruder's arrival. In addition, we tested the effect of the size of female reproductive tissue (measured in terms of egg load) and the quality of the habitat previously experienced by females (either rich or poor in hosts). These two factors are expected to influence the value that females place on the host and therefore the costs they are willing to pay to win it. Finally, we discussed the consequences of agonistic behaviors on females' host exploitation strategies. Our results suggest that contest competition may actually enhance host control by favoring parasitoid dispersion, rather than disrupting it.     

Effect of differential host exposure on reproduction in the solitary ectoparasitoid Eupelmus vuilleti

We examined self-superparasitism in Eupelmus vuilleti (CRW.), a solitary ectoparasitoid of larvae of Callosobruchus maculatus (F.) which develop in cowpea seeds. The reproduction of isolated females was analysed in the presence of seeds containing 10 or 30 hosts for 24, 48, and 72 h. At the two host densities, female reproductive activity increased with host exposure time, but variations in offspring number per female were limited. The propensity of the females to self-superparasitise their hosts after long exposure times could explain these results. The offspring sex ratio was female biased but tended to 0.5 for longer exposure times. The absence of host renewal for a 3-day period was followed by an increase in self-superparasitism which reduced the parasitoid survival rate and by emergence of a lower number of females in the offspring. The offspring production was then analysed when females were provided with ten hosts a day or with 30 hosts every three days throughout their life span. The reduction of host renewal frequency did not affect male production but caused a reduction in the number of females emerging from the seeds. The importance of a high rate of self-superparasitism on the population biology of this parasitoid is discussed.     

Sex allocation of three solitary ectoparasitic wasp species on bean weevil larvae: Sex ratio change with host quality and local mate competition

Sex ratio manipulation by ovipositing females was surveyed in 3 solitary ectoparastic wasp species,Dinarmus basalis (Pteromalidae),Anisopteromalus calanrae (Pteromalidae), andHeterospilus prosopidis (Braconidae), that parasitize azuki bean weevil (Callosobruchus chinensis (L) (Coleoptera: Buruchidae)) larvae within azuki beans (Vigna angularis). Variables were local mate competition (LMC) and host quality (HQ). We used host age as a measure of host quality (from 9-to 16-day-old hosts), changed the number of ovipositing females to control the level of local mate competition (1 female and 10 females), and examined oviposition patterns of the wasps. The offspring sex ratios (proportion of females) of the 3 wasp species respond qualitatively same to HQ and LMC. The common qualitative tendency among the 3 species is an increase of sex ratios increase with host age. In the process of changing the sex ratio (9–13-day-old) 3 wasp species respond only to HQ. In the hosts that end development in size (14–16-day-old) wasps respond to LMC. The response of sex ratio change to LMC in the old host ageclasses are different among the 3 species. In the situation that there exists LMC (10 females) sex ratios are the same among the 3 wasps. However, the sex ratios in no LMC (single female) are heterogeneous among the 3 wasps.     

Females of the weevil Zabrotes subfasciatus manipulate the size and number of eggs according to the host seed availability

Abstract. In some insects, the finding of oviposition substrate triggers the uptake into oocytes of yolk proteins that are stored in the fat body during post‐embryonic development. The main host of the bean weevil Zabrotes subfasciatus (Coleoptera; Chrysomelidae; Bruchinae; Amblycerini), in which larval resources are the sole source for future egg maturation, is Phaseolus vulgaris. Despite not feeding as adults, females of this species are able to lay eggs after encountering host seeds but it is not known how females react to changes in the availability of bean seeds. In the present study, the behaviour of Z. subfasciatus facing two very different environments for oviposition is investigated, as well as how this influences offspring fitness. The results obtained show that females of Z. subfasciatus react to variations in the availability of seeds belonging to the same host species by adjusting egg size and number. Females on low bean seed density lay larger and fewer eggs than those on high bean seed density, demonstrating a trade‐off between these reproductive traits. Moreover, females can adjust egg size to changing levels of host availability during the first 4 days of their oviposition period. Although no difference in offspring weight is found, those from small eggs (low competition environment) result in larger adults. No response to selection on these traits after rearing beetles on the same host for 40 generations is observed. This unresponsiveness may indicate that beetle populations behave according to their reaction norm that already allows rapid adaptation to a varying amount of host‐seed availability and better exploitation of the environments of this widespread stored‐seed pest.     

Behavioural and physiological responses to conflicting oviposition stimuli in a synovigenic parasitoid

The behavioural and physiological responses of the synovigenic parasitoid, Dinarmus basalis (Rond.) (Hymenoptera: Pteromalidae), were investigated whilst the wasps were submitted to conflicting oviposition stimuli: an environment which induced them to restrict egg-laying and a physiological factor, egg-load pressure, which induced them to lay eggs. When individual females depleted patches containing hosts parasitized 24 h or 72 h beforehand, they laid preferentially on unparasitized hosts and the number of eggs laid decreased significantly. Although they remained for several days in such patches, egg-load pressure did not lead them to modify their strategy (i.e. to accept all the available hosts including the already parasitized ones). In this synovigenic species, the oviposition constraint resulted in the retention of oocytes. Dissection and histological observation showed that the unlaid eggs are resorbed, a reproductive regulatory process which has seldom previously been reported in the presence of unparasitized hosts. This physiological response was induced by the mere presence of the parasitized hosts rather than their density. The females’ response was also influenced by the presence of conspecifics. They still avoided laying on parasitized hosts but the number of eggs laid daily became comparable to that observed in patches containing only unparasitized hosts. Thus, D. basalis females adapted their strategy in response to their environment, in which the most significant factor seemed to be the quality of the hosts provided, and their physiology. The originality and the importance of these results are discussed.     

Oviposition behavior and progeny allocation of the polyembryonic waspCopidosoma floridanum (Hymenoptera: Encyrtidae)

Oviposition behavior was used to determine the primary clutch size and sex ratio of the polyembryonic wasp Copidosoma floridanumAshmead (Hymenoptera: Encyrtidae) parasitizing Pseudoplusia includens(Walker) (Lepidoptera: Noctuidae). The laying of a female egg was associated with a pause in abdominal contractions during oviposition, while the laying of a male egg was associated with uninterrupted abdominal contractions. Although unmated females produced only male broods, they also displayed male and female egg oviposition movements. Wasps always laid a primary clutch of one or two eggs. For mated females if only one egg was laid, the emerging secondary clutch was all male or female, but if two eggs were laid a mixed brood of males and females was almost always produced. The secondary clutch of single sex broods was usually between 1000 and 1200 individuals, but the secondary clutch of mixed broods averaged 1143 females and 49 males. Thus, the primary sex ratio for mixed broods was 0.5 (frequency males), but the secondary sex ratio was 0.042. Manipulation of the sequence of male and female egg oviposition or of the primary clutch did not produce major alterations in the secondary clutch size or sex ratio.     

Biology of Australian and United States strains of Trissolcus basalis,a parasitoid of the green vegetable bug,Nezara viridula

Strains of Trissolcus basalis (Wollaston) Hymenoptera: Scelionidae, an egg parasitoid of the green vegetable bug, Nezara viridula (L.), were obtained from three regions of Australia and from Homestead, Florida (USA). Percent parasitoid emergence was approximately the same for freezer-stored (-75°C) and fresh eggs, and freezer-stored eggs were suitable hosts for a longer time. Optimum host age, oviposition and emergence patterns, mean number of progeny per female, sex ratio and longevity were examined and certain comparisons were made between the Australian and USA parasitoids. Genetic crosses made between males and females of each strain revealed that reproductive isolation did not occur. Higher fecundity of the Australian strains may make them more successful than indigenous (USA) strains for controlling pest populations of N. viridula in the southern USA.     

Impact of αAI-1 Expressed in Genetically Modified Cowpea on Zabrotes subfasciatus (Coleoptera: Chrysomelidae) and Its Parasitoid,Dinarmus basalis (Hymenoptera: Pteromalidae)

Genetically modified (GM) cowpea seeds expressing αAI-1, an α-amylase inhibitor from the common bean, have been shown to be immune against several bruchid species. Effective control of such pests by growing GM cowpea could promote the spread of bruchid species that are αAI-1 tolerant. Consequently, the sustainability of bruchid pest control could be increased by combining GM seeds and hymenopteran parasitoids. However, there are concerns that αAI-1 could interfere with the biological control provided by parasitoids. Here, we assessed the impact of GM cowpea seeds expressing αAI-1 on the αAI-1-tolerant bruchid Zabrotes subfasciatus and its parasitoid Dinarmus basalis. αAI-1 in cowpea seeds did not increase resistance to Z. subfasciatus or affect the mortality rate of Z. subfasciatus larvae. Parasitism of Z. subfasciatus by D. basalis and fitness of D. basalis offspring were not affected by the presence of αAI-1. Thus, αAI-1-expressing cowpeas and parasitoids should be compatible for the control of bruchid pests.     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Oviposition decisions in an endoparasitoid under self-superparasitism conditions

Superparasitism is a widespread phenomenon. Having accepted superparasitism, mated female parasitoids must decide on the sex of each egg they subsequently lay into the same host. Theory predicts that this decision is either based on host quality, when more male eggs are laid in hosts that are already parasitized because they are perceived to be of poorer quality; or more eggs are laid of the sex that is most likely to be a strong larval competitor, i.e. generally females.Anastatus disparis is a facultative endoparasitic egg parasitoid. We used ‘artificial’ hosts to explore outcomes of decision making by A. disparis during superparasitism under a manipulated absence of larval competition. When only one egg was laid it was always female. As the number of eggs laid increased, so more of them were male. This supports the theory that oviposition decisions are based on host quality; more male eggs were laid in hosts that were already parasitized and thus of poorer quality.In a second experiment, eggs were exposed to parasitoids for different periods of time. Half the eggs were dissected to determine the number of parasitoid eggs that had been laid. The remaining eggs were incubated and the number and sex of offspring that ultimately emerged, following larval competition, were recorded. Under superparasitism conditions fierce larval competition ensued; only one offspring survived and they were predominantly female.In conclusion, oviposition decisions by female A. disparis accepting self-superparasitism were made based on host quality.     

Parasitism of aphid embryos by Aphidius smithi: some effects of extremely small host size

Embryos of the pea aphid, Acyrthosiphon pisum (Harris), were successfully parasitized by Aphidius smithi Sharma & Subba Rao while still inside their mother. Parasites from embryos were much smaller, laid fewer eggs, but survived as long as their counterparts that had developed in adult viviparous aphids. Lifetime fecundity was positively correlated with wasp size, as measured by dry weight at the time of death. A. smithi females produced the same offspring sex ratio at eclosion on both host classes, although emergence was significantly lower from mummified adult aphids than from embryos. The data are discussed with regard to progeny and sex allocation decisions by solitary hymenopterous parasites. It is suggested that, in A. smithi, the decision to lay a fertilized or unfertilized egg is influenced by the host's overall size, rather than by the size and quality of a smaller target area inside the host, such as embryos.